Community structure, trophic ecology and reproductive mode of oribatid mites (Oribatida, Acari) in forest
ecosystems
Dissertation zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultäten der
Georg-August-Universität Göttingen
vorgelegt von Diplom-Biologin
Georgia Erdmann
aus Räckelwitz
Göttingen, März 2012
S
B
IODIVERSITÄT, Ö
KOLOGIE UNDN
ATURSCHUTZ− CE NTRE OF BI ODI VERS I TY A ND SUS TA INA BL E LA ND USE − SE CTI ON: BI ODI V E RS I TY, ECOL OGY A ND NA TURE CONS E RVA TI ON
Referent: PD Dr. Mark Maraun Koreferent: Prof. Dr. Stefan Scheu Tag der mündlichen Prüfung: 26.03.2012
Summary ... 1
Reference ... 3
Chapter 1 General Introduction ... 4
1. Density, diversity and distribution of oribatid mites ... 5
2. Functioning and trophic ecology of oribatid mites ... 6
3. Reproduction and life-history traits ... 7
4. Systematics of oribatid mites ... 8
5. Oribatid mites as model organisms ... 9
6. Theories about the maintenance of sexual reproduction... 10
7. Overview ... 11
References ... 14
Author Contributions ... 19
Chapter 2 Stable isotopes revisited: their use and limits for oribatid mite trophic ecology ... 20
Abstract ... 21
1. The history of the use of stable isotopes in soil food web analysis ... 21
2. Uncovering the trophic structure of oribatid mite communities ... 23
3. Recent progress ... 25
4. Challenges for the future ... 29
5. Limitations and caveats ... 31
Acknowledgements……….……….32
References ... 32
Appendix ... 36
Regional factors rather than forest type drive the community structure
of soil living oribatid mites (Acari, Oribatida) ... 37
Abstract ... 38
1. Introduction ... 38
2. Materials and Methods ... 40
2.1. Study sites ... 40
2.2. Sampling design... 40
2.3. Environmental factors ... 41
2.4. Statistical analysis... 41
3. Results ... 42
3.1. Oribatid mite density ... 42
3.2. Species numbers of oribatid mites ... 43
3.3. Community structure of oribatid mites ... 44
4. Discussion ... 47
4.1. Oribatid mite density ... 47
4.2. Oribatid mite diversity ... 48
4.3. Oribatid mite community structure ... 49
4.2. Conclusions ... 50
Acknowledgements ... 50
References ... 51
Appendix ... 55
Chapter 4 Positive correlation between density and parthenogenetic reproduction in oribatid mites (Acari) supports the structured resource theory of sexual reproduction ... 56
Abstract ... 57
1. Introduction ... 57
2. Materials and Methods ... 60
3. Results ... 64
3.1 Regional scale ... 64
3.2 Global scale ... 65
4. Discussion ... 66
4.1 Parthenogenetic reproduction in oribatid mites ... 66
4.2 Regional scale ... 67
4.3 Global scale ... 67
4.4 The structured resource theory of sexual reproduction as an integrative theory .. 68
Acknowledgements ... 69
References ... 69
Literature used for the meta-analysis ... 72
Appendix ... 74
Chapter 5 Oribatid mite (Acari, Oribatida) density on tree trunks is regulated by food-resources ... 81
Abstract ... 82
1. Introduction ... 82
2. Materials and Methods ... 84
2.1 Study sites ... 84
2.2 Sampling design... 85
2.3 Statistical analysis... 86
3. Results ... 86
3.1 Density ... 86
3.2 Community structure ... 87
3.3 Stable isotopes ... 88
4. Discussion ... 89
Acknowledgements ... 91
References ... 91
Appendix ... 95
General discussion ... 96
1. Stable isotope analysis of soil- and bark-living oribatid mites ... 98
2. Effect of forest types on oribatid mites ... 99
3. Frequency of parthenogenetic oribatid mites related to resources in soils ... 101
4. Tree trunks – a resource-limited habitat for oribatid mites ... 102
5. Conclusions ... 103
References ... 104
Acknowledgements ... 108
List of publications ... 109
Thesis Declaration ... 110
Summary
Oribatid mites are predominantly soil-living organisms reaching densities of up to 400,000 individuals per square meter in forest soils, where they contribute to decomposition processes and nutrient cycling. In acidic forests they are the main decomposer taxon, together with collembolans. Despite their outstanding importance for soil processes knowledge about their trophic ecology and factors structuring their communities is low.
About ten percent of the 10,000 described species are thelytokous (i.e., they reproduce via female parthenogenesis); locally up to 80 % of all individuals in temperate forest soils are parthenogens. Oribatid mites likely originated in Cambrian or Precambrian times and include old thelytokous species-rich groups indicating an ancient origin of asexuality as well as parthenogenetic radiations. Sexual and parthenogenetic species coexist in forest soils and in agricultural soils; in temperate, tropical and arctic regions and also on the bark of dead and living trees. This makes oribatid mites a unique group for studying patterns of parthenogenetic reproduction and for studying factors influencing the relative frequency of sexual and parthenogenetic species (see Chapter 1).
The present thesis focuses on oribatid mite reproductive mode and ecology and is divided into two parts. The first part investigates the trophic ecology of oribatid mites in soil and on bark analysed with stable isotope measurements (Chapter 2) and abiotic and biotic factors influencing oribatid mite density, diversity and community structure in soils of different forest types (Chapter 3). In the second part oribatid mites were used as model organisms to investigate the distribution of sexual and parthenogenetic individuals in forest soils in two regions in Germany and in different habitats worldwide in relation to food availability (Chapter 4). Further we investigated the effects of nutrient availability on oribatid mite density and the frequency of parthenogenetic individuals on tree trunks (Chapter 5).
In Chapter 2 we used two stable isotopes (15N; 13C) for uncovering the trophic ecology of soil- and bark-living oribatid mites. The isotope 15N is usually used to detect the trophic level in food webs since it is enriched by about 3.4 delta units per trophic level, whereas 13C can be a marker for different food sources since different food source s can differ in their 13C signatures (e.g., lichens, C4 and C3 plants), but those signatures are not enriched per trophic levels. It could be shown that oribatid mites span over four trophic levels, which was surprising since usually oribatid mites are treated in food webs as a single functional group, i.e., decomposers. However, our data clearly show
that oribatid mites are a trophically diverse group and should not be aggregated in food webs.
Additionally, 13C signatures separated lichen feeders as well as species that burrow inside leaves and needles as juveniles (endophagous taxa) from the other species.
In Chapter 3 we investigated the importance of regional versus local factors on oribatid mite community structure. Therefore, we studied oribatid mites in four differently managed forest types (coniferous 70y old age class forests; 30y old and 70y old beech age class forests, unmanaged beech forests mature with trees ~120y old) (local effects) at three different sites in Germany (Swabian Alb, Hainich, Schorfheide) (regional effects) in the framework of the DFG project “Biodiversity Exploratories”. We also measured environmental factors (litter mass, soil pH, C and N content of litter and fine roots, C content of soil) which might potentially explain oribatid mite density and community structure. Oribatid mite density was positively correlated with litter mass supporting the hypothesis that the litter serves as a habitat and also as a food resource for many oribatid mite species. Oribatid mite diversity was little affected by forest type indicating that in most forest types the number of niches for oribatid mites is similar. Overall, differences of oribatid mite communities were more pronounced between the three regions than between the four forest types within a region indicating that regional factors (mainly pH, litter mass and C content of litter) are more important than local factors for oribatid mite community structure. Overall, the predictability of density, diversity and community structure of oribatid mite communities in different regions indicates that oribatid mite communities are not randomly assembled.
In Chapter 4 we investigated the hypothesis that parthenogenetic species should dominate in habitats with a good food supply where resources are not a limiting factor. In contrast, in habitats where resources are in short supply or strongly structured sexual reproduction should dominate since mixis processes potentially allow a better use of underutilized resources (”Structured Resource Theory of Sexual Reproduction” (SRTS); Scheu and Drossel 2007). Our data show a strong positive relationship between parthenogenetic reproduction and density (which we used as an indirect measurement for resource availability) supporting the hypothesis that availability of food in ample supply triggers parthenogenesis and allows the long-term maintenance of parthenogenetic reproduction.
In Chapter 5 we experimentally investigated the hypothesis that increased resource availability increases the density of oribatid mites and also the prevalence of parthenogens. For this study we added nutrients in the form of cane sugar as a carbon source (C) and ammonium nitrate as a nitrogen source (N) on the tree trunks of beech trees (Fagus sylvatica). Oribatid mite density increased after C addition supporting the view that oribatid mites on the bark of trees are resource limited. However, the number of parthenogenetic individuals did not increase after resource addition (neither C or N)
which was mainly due to the fact that the bark is a habitat where sexual taxa dominate (~95 %).
Migration of parthenogens from soil obviously was too low to affect community sex ratios.
Reference
Scheu, S., Drossel, B. (2007) Sexual reproduction prevails in a world of structured resources in short supply. Proceedings of the Royal Society B – Biological Sciences 274, 1225-1231.
1. Density, diversity and distribution of oribatid mites
Oribatid mites are typical soil living microarthropods reaching densities of up to 200,000 individuals per square meter in acidic raw humus of coniferous forests (Maraun and Scheu 2000). With increasing soil pH oribatid mite densities decrease to ~ 20,000-60,000 individuals per square meter in mull soils of deciduous forests (Maraun and Scheu 2000). They are also common in agricultural soils, such as pastures and fields, but have lower densities of ~ 10,000 individuals per square meter (Maraun and Scheu 2000). Living in almost all terrestrial habitats from deserts to polar regions, from fresh water to saltmarshes (Walter and Proctor 1999), oribatid mites are among the most abundant microarthropods in soil. Furthermore, oribatid mites also colonize a huge range of microhabitats including the surface of stones, lichens (Travé 1963, Gjelstrup and Sochting 1979), dead wood (Aoki 1967), tree trunks (Erdmann et al.
2006) and suspended soils in tree crowns (Lindo and Winchester 2007).
About 10,000 species of oribatid mites are described worldwide (Subias 2004, Schatz 2005) and a total number of 110,000 species is estimated to exist (Walter and Proctor 1999). On a global scale, diversity is lowest in Antarctica with 27 species (Stary and Block 1998) and increases with decreasing latitude being highest in boreal and the warm temperate regions, but does not increase further to the tropics (Maraun et al. 2007). In Germany 520 oribatid mite species are documented (Weigmann 2006) with typical numbers of 50-120 species in soil of single forests (Wunderle 1992, Norton and Behan-Pelletier 2009). Despite the seemingly homogeneous habitat soil organisms live in, the diversity of soil animals is very high (Giller 1996). This phenomenon has been termed the “enigma of soil animal diversity” (Anderson 1975).
Overall density and community composition at the level of morphological and functional groups is predictable over a broad range for habitat types (Maraun and Scheu 2000). Caruso et al. (2011) investigated the dissimilarity of oribatid mite communities in two habitats (Mediterranean beech forest and grassland) at different geographical distances (from centimeters to tens and hundreds of meters). To a large extent the variation in oribatid mite community composition in space was independent of measured environmental variables (e.g., organic matter), but the dissimilarity of the communities did not match predictions of neutral models. The results suggest that both stochastic and deterministic processes contribute to oribatid mite assemblage structure.
The importance of bottom-up or top-down forces on oribatid mite communities is unclear and still debated (Salamon et al. 2006, Lenoir et al. 2007, Schneider and Maraun 2009).
Predators of oribatid mites range from small vertebrates e.g., salamanders (Norton and McNamara 1978) and frogs (Saporito et al. 2007), over centipedes (Lebrun 1970) and insects, e.g., Scydmaenidae (Schuster 1966) and Formicidae (Wilson 2005), to other mites e.g,.
Prostigmata and Mesostigmata (Wallwork 1980, Peschel et al. 2006). However, the impact of predation - at least for adult oribatid mites - is likely to be of minor importance. Oribatid mites are regarded as living in an enemy-free space due to chemical defense (Heethoff et al. 2011) and strongly hardened cuticle, but the latter is less pronounced in juveniles (Peschel et al.
2006). Perturbations have been shown to detrimentally affect oribatid mites (Maraun et al.
2003). Especially earthworms exert strong negative impacts on oribatid mite communities (Migge-Kleian et al. 2006, Eisenhauer 2010) which likely is due to litter comminution and mixing of litter and soil.
2. Functioning and trophic ecology of oribatid mites
Oribatid mites are predominantly decomposers, feeding on dead organic material and fungi.
Especially in acidic soils (where earthworms are absent), oribatid mites carry out important decomposition processes (Lussenhop 1992) and play an important role in nutrient cycling, mineralization processes and humus formation (Krantz 2009). Further, they distribute fungal spores and bacteria that are attached to their body surface or transported in their gut which supports fungal colonization of dead organic material and decomposition processes (Maraun et al. 1998, Renker et al. 2005).
Different approaches, such as gut content analysis (Hubert et al. 2001), analysis of enzyme activities (Siepel and deReuiter-Dijkmann 1993), measuring of cheliceral sizes (Kaneko 1988) and laboratory feeding experiments (Schneider et al. 2005, Koukol et al. 2009), resulted in different systems of distinct feeding categories. Schneider et al. (2004) investigated stable isotope signatures of oribatid mites in soil and demonstrated that species feed in a continuous range of three to four trophic levels including phycophages/fungivores (lichen and algae), primary decomposers (predominantly feeding litter), secondary decomposers (predominantly consuming fungi and in part litter) and carnivores/scavengers/omnivores (feeding on living and dead animals, e.g., nematodes (Heidemann et al. 2011), springtails and potentially mycorrhizal fungi).
Recent studies postulated that oribatid mites heavily rely on rhizosphere carbon (Pollierer et al. 2007). Additional micro habitats extend the variety of food resources oribatid mites feed on; e.g., oribatid mites on bark mainly feed on lichens and algae (Erdmann et al. 2007, Fischer et al. 2010a).
3. Reproduction and life-history traits
Oribatid mites are diplodiploid organisms with presumably holokinetic chromosomes (Norton et al. 1993). Females can easily be distinguished from males (Grandjean 1955, 1956) since females have a large ovipositor with a typical wavelike surface pattern. There are three pairs of genital papillae on the basis of the ovipositor. Throughout the year females carry eggs inside the notogaster. All three structures, ovipositor, genital papillae and eggs, can easily be seen under a microscope. The spermatophore depositor of the male is rather small and more difficult to see than the ovipositor.
Sperm transfer usually takes place indirectly via stalked spermatophores. Eggs are laid in crevices, where they develop from prelarvae, larvae, deutonymphs and tritonymphs to adult organisms. Lifetime fecundity of oribatid mites is low, compared to other mite groups (Norton 1994). They are considered as K-strategists with delayed maturity, low reproductive potential, iteroparity and long adult life (Norton 1994). The variation in generation times is high and fecundity differs seasonally. The species Oppiella nova carries single eggs and lays upto twelve eggs per week in culture (Woodring and Cook 1962) while Steganacarus magnus carries about six eggs and lays them at lengthy intervals (Webb 1989). Under laboratory conditions females of some species lay between six and twelve eggs during livetime (Nothrus biciliatus; Saichuae et al. 1972), whereas other females lay up to 250 eggs in a single year (Platynothrus peltifer;
Grandjean 1950). Developmental rates vary in soils of the temperate zone between several months to over a year (Norton 1994). Sexual species had higher number of eggs than parthenogenetic species in laboratory experiments (Domes et al. 2007b). However, the total reproductive rate depends on generation time, mode of reproduction and number of eggs produced and is little understood (Domes et al. 2007b). Species with wide ecological distributions show a high degree of plasticity of life cycle duration with an elongation under cold conditions (Norton 1994).
Interestingly, ten percent of the approximately 10,000 described oribatid mite species (Subias 2004, Schatz 2005) are thelytokous i.e., females produce daughters from diploid eggs without fertilization by males. No males or very few non-functional (spanandric) males exist
which do not genetically contribute to the next generation (Grandjean 1941, Taberly 1988, Palmer and Norton 1992, Norton et al. 1993).
The classification of parthenogenetic species was carried out on the basis of rearing experiments or is suspected from the absence or rarity of males in natural populations (Norton et al. 1993). While sexual species have a sex ratio of approximately 1:1 (lowest recorded sex ratio of 1/4.4; Luxton 1981), the proportion of females in parthenogenetic species is 95-100 % (Norton and Palmer 1991, Palmer and Norton 1992, Cianciolo and Norton 2006, Domes et al.
2007a). Cyclical or geographic parthenogenesis is not known for oribatid mites (Norton and Palmer 1991).
Meiotic processes are involved in the reproductive mechanism. Automoxis with terminal fusion is probably the most common mechanism (Taberly 1987, Heethoff et al. 2006), but central fusion automixis and apomixis were proposed to explain the fixed heterozygosity which was found for nine oribatid mite species using isozyme techniques (Palmer and Norton 1992), but were not confirmed by molecular data of elongation factor (ef1α) and heat-shock protein (hsp82) (Schaefer et al. 2006). Wrensch et al. (1994) suggested inverted meiosis of holokinetic chromosomes to explain the occurrence of terminal fusion in combination with heterozygosity.
4. Systematics of oribatid mites
Mites belong to the Arthropoda and represent the most diverse and extant ancient lineage of the Chelicerata (Walter and Proctor 1999). The major taxa are Opilioacariformes, Parasitiformes (with Mesostigmata, Holothyrida and Ixodida) and Acariformes (including Sarcoptiformes, Trombidiformes and Endeostigmata) (Walter and Proctor 1999). Oribatid mites belong to the Sarcoptiformes and are classified into six groups according to morphological characters: the species-poor and basal Palaeosomata (weak sclerotization), the Enarthronota (transversal line on notogaster), Parhyposomata (continuous notogaster shield), paraphyletic Mixonomata (dichoid; with separated Proterosoma and Hysterosoma), paraphyletic Desmonomata (holoid) and species-rich Circumdehiscentia = Brachypylina (spatially separated genital and anal plate in a fused ventral shield) (Walter and Proctor 1999).
Molecular analyses date the origin of oribatid mites back to the Precambrian (571 ±37 mya) and, therefore, they may represent an early component of terrestrial food webs (Schaefer et al. 2010).
Species-rich and exclusively parthenogenetic clades exist within the oribatid mites pointing to ancient asexuality and parthenogenetic radiations (Norton et al. 1993). This renders oribatid mites, next to bdelloid rotifers and darwinulid ostracods (which also radiated while being parthenogenetic) so called “evolutionary scandals” (Maynard Smith 1978). Parthenogenetic reproduction should result in evolutionary short-lived lineages and is assumed to be an evolutionary dead end (Maynard Smith 1978) due to the accumulation of deleterious mutations (Muller 1964, Kondrashov 1993) and/or a reduced adaptative potential to changing environments (Ghiselin 1974, Bell 1982).
5. Oribatid mites as model organisms
Oribatid mites are a suitable model organism for investigations of evolutionary processes (Norton and Palmer 1991, Schaefer et al. 2006, Domes et al. 2007a, Heethoff et al. 2009), but also for studying ecological aspects of parthenogenesis. Parthenogenetic and sexual oribatid mites coexist with different frequencies in a wide range of habitats. Parthenogenetic taxa, such as Brachychthoniidae, Oppiella nova and Tectocepheus spp., dominate in new or disclimax habitats (Norton and Palmer 1991), but occur in lower proportions also in climax habitats (Maraun and Scheu 2000). The proportion of parthenogenetic individuals, e.g., in Eulohmanniidae, Brachychthoniidae, Oppiidae and certain Epilohmanniidae, increases with increasing soil depth (Luxton 1982, Norton and Palmer 1991). Fresh water habitats are inhabited by parthenogenetic species, such as of Thrypochthoniidae; Malaconothridae, Limnozetidae and certain Hydrozetes spp. (Norton and Palmer 1991). Marine habitats are mainly inhabited by sexual species (Schuster 1979), such as Ameronothrus spp. and Halozetes spp. (Proches and Marshall 2001).
Oribatid mites primarily live in soils, but also on the bark of trees. In forest soils of the temperate zone they comprise of 58 % to 87 % parthenogenetic individuals (Maraun et al.
2003, Fischer et al. 2010a), while on the bark of tree trunks only 1-15 % of oribatid mites belong to parthenogenetic species (Erdmann et al. 2006, Fischer et al. 2010a). The proportion of parthenogenetic individuals fundamentally changes in a range of a few centimeters between forest soil and tree trunk. Investigating these patterns and indentifying the basic ecological factors and mechanisms which are responsible for the distribution of parthenogenetic and sexual oribatid mites is a promising approach to start solving the mystery of ecological advantages of sexual and parthenogenetic reproduction.
6. Theories about the maintenance of sexual reproduction
In the last decades more than 25 hypotheses were developed trying to identify major factors which explain the dominance of sexual reproduction in animal taxa (Kondrashov 1993, Schoen 2009). These theories differ with regard to the key factors triggering sexual reproduction, e.g., temporal or spatial variation, resource availability or parasitism rate, short- or long-term advantages (West et al. 1999, Scheu and Drossel 2007) and explain only parts of the ecological distribution of parthenogenetic reproducing organisms. Maynard Smith (1976) wrote “one is left with the feeling that some essential feature of the situation is being overlooked”.
The two most common hypotheses are the ‘Tangled Bank’ and the ‘Red Queen’. The focus of the ‘Tangled Bank theory’ is a spatially heterogeneous environment in which the brake-up of locally favorable gene-combinations reduces sib-competition and may be advantageous for a better exploitation of resources in enclosed habitats (Williams 1975, Bell 1982). The ‘Red Queen theory’ focuses, in contrast to the ‘Tangled Bank theory’, on a temporally heterogeneous environment. Predators and parasites are adapted to prey on genotypes with highest frequencies. Sexual species produce genetically variable offspring which may be resistant against parasites or which may avoid or escape from predators (Glesener 1979, Hamilton 1980, Stearns 1985).
Scheu and Drossel (2007) developed a model on the maintenance of sexual reproduction, integrating spatially and temporally variation - the ‘Structured Resource Theory of Sexual Reproduction’ (SRTS). The fundamental assumption of the SRTS is the availability of limited amounts of resources for a population with a limited number of genotypes consuming only part of these resources Thereby depleting this fraction of the resources available for the next generation. Sexual offspring can better exploit underutilized resources and outcompete asexual ones. The model differentiates explicitly between (a) biotic and abiotic density- dependent factors and (b) physicochemical density-independent factors. These assumptions lead to predominance of asexual reproduction (1) in habitats with an excess of resources (no adaptation to limited resources needed) (2) in habitats with a small number of resources (3) in populations with a high number of genotypes which are able to exploit all possible resources to the same extent or (4) in habitats with strong density-independent effects, such as harsh, disturbed or novel environments (effects are unpredictable, individuals cannot adapt to these effects; resources are never fully exploited (Scheu and Drossel 2007)).
7. Overview
This study consists of two main parts. The first part introduces the ecology of oribatid mites (Chapter 2 and 3) and presents data on trophic ecology and ecological factors which structure oribatid mite communities in temperate forest soils. In the second part (Chapter 4 and 5) oribatid mites were used as model organisms to test the predictions of the SRTS on the distribution of parthenogenetic individuals in below- and aboveground habitats.
The oribatid mite diversity in forest soils is high; disentangling feeding niches may help to explain this phenomenon. Furthermore, availability of food resources is the basic feature in the SRTS of Scheu and Drossel (2007) and raises the question what kind of food resources oribatid mites consume. The investigation of trophic and feeding ecology of oribatid mites is challenging since they are tiny and the opaqueness of their habitat makes direct observations difficult. In the last years considerable progress has been made using the method of stable isotope analysis allowing novel insights into the trophic ecology of oribatid mites. Chapter 2 reviews the trophic ecology of oribatid mites using the method of stable isotopes, summarizes previous results, gives perspectives for future studies and presents new data on the trophic structure of oribatid mite communities in forest soils for 26 species, compared with stable isotope data of 7 oribatid mite species from tree trunks (tree trunk data from Fischer et al.
2010a). Oribatid mites in soil span three to four trophic levels and differ in their δ15N values compared to bark-living oribatid mites indicating feeding-niche differentiation in soil and between habitats. The additional analysis of δ13C provided additional informations on trophic niches. Taxa with endophagous juveniles were recognizable from other oribatid mites by enriched δ13C values. Lichens and oribatid mites diverged strong in their δ13C values and showed that bark-living oribatid mites feed mainly on lichens and not on mosses.
In Chapter 3 the importance of biotic and abiotic environmental factors and their influence on density, diversity and the structure of oribatid mite communities in coniferous forests (Picea abies or Pinus sylvestris; depending on the study site); beech forests (Fagus sylvatica; 30 y and 70 y old) and unmanaged beech forests was studied. The four forest types were replicated in three regions in Germany, spanning a latitudinal gradient of ~500 km. The study design allowed general conclusions on structuring factors for oribatid mite density, diversity and community composition in the four forest types. The investigated tree species and management types are most common and typical for Central Europe. We suspected highest densities in coniferous forests due to thick litter layer and highest diversity in old unmanaged forests due to increased habitat heterogeneity. Oribatid mite densities decrease from coniferous over 30 y and 70 y old beech forests to the unmanaged beech forests and were
correlated positively with the mass of litter layer and negatively with soil pH. Diversity of oribatid mites was little affected by forest type indicating that they harbor similar numbers of niches. The oribatid mite community structure differed more between the three regions than between the four forest types indicating the importance of regional factors rather than factors associated with forest types. Soil pH, which is a factor resulting from regional geological conditions and local forest types, strongly affected the oribatid mite communities.
In Chapter 4 one prediction of the SRTS was tested for soil-living oribatid mites. Habitats with an excess of resources should be dominated by asexual organisms because adaptation to limited resources is not needed. That means, the proportion of parthenogenetic oribatid mites should increase with increasing availability of resources. The amount of food resources was estimated indirectly since food sources of oribatid mites are only partially known and their amount in soil is hardly detectable. Increased densities and respiration values of oribatid mites per square meter were assumed to indicate increased resource availability. An increase in the proportion of parthenogenetic oribatid mites with increasing densities or respiration of oribatid mites per square meter would support the assumption of the SRTS. The correlation of the proportion of parthenogenetic oribatid mites with densities or respiration of oribatid mites per square meter was tested and compared on the small scale (two regions in Germany:
Schorfheide and Swabian Alb), as well as on the large scale (worldwide) in a meta analysis. The assumption of the SRTS was supported in the small scale and in the large scale analysis.
Overall, oribatid mite densities correlated positively with the proportion of parthenogenetic individuals. Locally, the density and respiration of oribatid mites correlated significantly with the proportion of parthenogenetic individuals in Schorfheide, but not in the Swabian Alb. High densities of earthworms in the Swabian Alb may superimpose the effects of food-resources on oribatid mites compared with Schorfheide with low earthworm densities.
The effect of resource availability on oribatid mite densities and on the proportion of parthenogenetic individuals was investigated on the bark of tree trunks in Chapter 5. One prediction of the SRTS is the prevalence of parthenogenesis in habitats with strong density- independent effects, such as harsh, disturbed or novel environments (Scheu and Drossel 2007). The bark of tree trunks is considered as harsh environment affected by desiccation, frost and solar radiation. In contrast to those theoretical expectations, the bark of tree trunks is dominated by sexual oribatid mite species (Erdmann et al. 2006, Fischer et al. 2010a). The SRTS states that sexual reproduction should dominate in habitats where resources are limited or little accessibly. The resource availability on tree trunks was manipulated by monthly fertilization of bark with nitrogen (N), carbon (C), both (N and C) and water as control. An
fertilization would indicate resource limitation rather than limitation by harsh abiotic conditions as predicted by the SRTS. The uptake of fertilizers by oribatid mites was evaluated using stable isotopes (14N/15N; 12C/13C). Oribatid mite densities increased in treatments with C fertilization. The fertilization with N had no effect. This is in accordance with stable isotope data indicating the incorporation of C but not of N of the fertilizers in the tissue of oribatid mites. The increase in oribatid mite densities due to C fertilization indicates food resource limitation on bark and supports the suggestions made by the SRTS.
All studies were conducted in the framework of the Biodiversity Exploratories (www.Biodiversity-Exploratories.de), a long-term and large-scale project investigating forest and grassland sites, established in three regions in Germany (the Swabian Alb, the Hainich and the Schorfheide-Chorin). The aim of the Biodiversity Exploratories is the investigation of the role of land use and management on biodiversity, ecosystem functions and services (Fischer et al. 2010b)
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Author contributions
Chapter 2: Stable isotopes revisited: Their use and limits for oribatid mite trophic ecology Authors: M. Maraun, G. Erdmann, B.M. Fischer, M.M. Pollierer, R.A. Norton, K. Schneider, S.
Scheu
Published in Soil Biology & Biochemistry (2011), Volume 43, Issue 5, Pages 877-882.
Contributions: Idea by M.M., R.A.N., S.S., K.S. & G.E.; empirical data from G.E., B.M.F., K.S. &
M.M.P.; analysis by M.M. & G.E.; text written by M.M., G.E., S.S. & M.M.P.
Chapter 3: Regional factors rather than forest type drive the community structure of soil living oribatid mites (Acari, Oribatida)
Authors: G. Erdmann, S. Scheu, M. Maraun
Published in Experimental and Applied Acarology (2012), Volume 57, Issue 2, Pages 157-169.
Contributions: Idea by M.M., S.S. & G.E.; empirical data from G.E.; analysis by G.E.; text written by G.E., S.S. & M.M.
Chapter 4: Positive correlation between density and parthenogenetic reproduction in oribatid mites (Acari) supports the structured resource theory of sexual reproduction
Authors: M. Maraun, R.A. Norton, R.B. Ehnes, S. Scheu, G. Erdmann
Published in Evolutionary Ecology Research (2012), Volume 14, Number 4, Pages 311-323.
Contributions: Idea by M.M. & S.S.; empirical data from M.M. & G.E.; analysis by M.M., G.E. &
R.B.E.; text written by M.M., S.S. & G.E.
Chapter 5: Oribatid mite density (Acari, Oribatida) on tree trunks is regulated by food resources – confirming the “Structured Resource Theory of Sexual Reproduction”
Authors: G.Erdmann, S. Scheu, M. Maraun In preparation
Contributions: Idea by M.M., S.S. & G.E.; empirical data from G.E.; analysis by G.E. & M.M.; text written by G.E., S.S. & M.M.
Abstract
In this review we summarize our knowledge of using stable isotopes (15N/14N, 13C/12C) to better understand the trophic ecology of oribatid mites. Our aim is to (a) recapitulate the history of stable isotope research in soil animals with a focus on oribatid mites, (b) present new stable isotope data for oribatid mites and the current state knowledge of oribatid mite trophic niche differentiation, (c) compile problems and limitations of stable isotope based analyses of trophic relationships and (d) suggest future challenges, questions and problems that may be solved using stable isotope analyses and other novel techniques for improving our understanding on the trophic ecology of soil invertebrates. We conclude that (1) in addition to 15N/14N ratios, 13C/12C ratios contribute to our understanding of the trophic ecology of oribatid mites, allowing e.g., separation of lichen- and moss-feeding species, (2) there likely are many lichen but few moss feeding oribatid mite species, (3) oribatid mite species that are endophagous as juveniles are separated by their stable isotope signatures from all other oribatid mite species, (4) fungivorous oribatid mite species cannot be separated further, e.g., the fungal taxa they feed on cannot be delineated. A particular problem in using stable isotope data is the difficulty in determining signatures for basal food resources since decomposing material, fungi and lichens comprise various components differing in stable isotope signatures; 13C/12C ratios and potentially other isotopes may help in identifying the role of these resources for decomposer animal nutrition.
1. The history of the use of stable isotopes in soil food web analysis
Terrestrial soil ecologists came rather late to the use of stable isotope ratios (mainly 15N/14N and 13C/12C) to analyze the structure of food webs. When we started with our now frequently- cited study about stable isotope ratios (15N/14N) in soil-living oribatid mites (Schneider et al.
2004) in 2003, stable isotopes had been used for decades to study trophic relationships in marine (Minagawa and Wada 1984, Sholto-Douglas et al. 1991) and freshwater systems (Gu et al. 1994, Hall 1995). In soil systems the seminal papers by Ponsard and Arditi (2000) and Scheu and Falca (2000) used stable isotopes (15N/14N and 13C/12C) for the first time to analyze the trophic structure of soil animal food webs in a comprehensive way. The results of these two studies indicated that food chains in soil are rather short, with decomposers being clearly separated from predators, but they suggested strong variation in the trophic position of species of both decomposers and predators.
Stable isotopes have been used not only to study trophic levels in food webs but also to investigate the trophic ecology of specific taxonomic groups, e.g., earthworms (Martin et al.
1992), seabirds (Hobson et al. 1994), pinnipeds (Hobson et al. 1997), amphibians (Altig et al.
2007) and lizards (Struck et al. 2002). Their application to soil animals started in the 1980s with the investigation of termites (Boutton 1983, Tayasu 1998) and was continued by studies on ants (Blüthgen et al. 2003) and earthworms (Schmidt and Ostle 1999). The results indicated marked trophic niche separation of the respective species. It was not until 2004 that stable isotopes were used to delineate trophic niches of a major group of putatively saprophagous soil mesofauna, the oribatid mites (Schneider et al. 2004), and one year later this study was followed by a similar investigation of Collembola (Chahartaghi et al. 2005). A third study focusing on the predatory soil mesofauna, i.e. mesostigmate (gamasid) mites, is pending (B.
Klarner, unpublished data).
Only nine species of oribatid mites were included in the stable isotope study of Scheu and Falca (2000) and none in that of Ponsard and Arditi (2000). Therefore, in Schneider et al.
(2004) we chose to investigate the stable isotope ratios (15N/14N) of oribatid mite species of forests in a comprehensive way, by including all major taxa and comparing different forests.
Further, for investigating variations in stable isotope ratios between habitats and between developmental stages we included oribatid mites from different microhabitats, e.g.,, the bark of trees, and analyzed both adults and juveniles of some species. For delineating the baseline, potential food resources of decomposer species were investigated.
The use of stable isotopes for studying food webs was introduced by DeNiro and Epstein (1981), Minagawa and Wada (1984) and Wada et al. (1991). They found that the trophic structure of animal communities can be evaluated by analyzing the natural variation in 15N/14N and 13C/12C ratios. On average, animal tissues are enriched in 15N compared with their food source by about of 3.4 δ units per trophic level and in 13C by about 1 δ unit (Post 2002). This allows fast and standardized evaluation of the trophic structure of animal food webs even if little is known of predator - prey relationships. This is particularly advantageous for analyzing food web structure of cryptic communities like those in soil. Stable isotope analysis is particularly powerful in opening the structure of soil animal food webs if combined with other recently developed methods for analyzing food webs, such as fatty acid analysis (Chamberlain et al. 2004, Ruess et al. 2004, 2005a) and molecular gut content analysis (King et al. 2008), as these methods allow closer identification of trophic links. Similar to fatty acid analysis, but in contrast to molecular gut content analysis, stable isotope ratios of animal tissue reflect nutrition over long periods of time, allowing the delineation of general characteristics of the
trophic structure of food webs. Further, variations in 13C/12C ratios of food resources, e.g., between C3 and C4 plants, allow us to trace the transfer of carbon from major resources through animal food webs (Oelbermann et al. 2008, Pringle and Fox-Dobbs 2008).
2. Uncovering the trophic structure of oribatid mite communities
The analysis of the stable isotope ratios of nitrogen (15N/14N) and carbon (13C/12C) has contributed significantly to our understanding of the trophic structure of soil animal taxa and this started with the detailed analysis of oribatid mites (Schneider et al. 2004). First and most important, this study showed that stable isotope ratios of nitrogen in this single taxonomic group of soil invertebrates vary to an extent that was entirely unexpected. In fact, the results indicated that oribatid mites span about four trophic levels, similar to what had been suggested previously for the total invertebrate soil animal food web of deciduous forests (Scheu and Falca 2000). This is highly incongruent with the common practice of lumping oribatid mites into a single trophic group and indicates that soil food webs based on such coarse taxonomic units lack realism and represent caricatures of nature.
Early studies based on physical gut content analyses and direct observation had already suggested that "mycophagous" soil invertebrates like oribatid mites in fact are trophically diverse and include species living as predators, scavengers, algal and lichen feeders (e.g., Walter 1987), but the findings remained somewhat anecdotal and were largely ignored. Using stable isotope analysis, and analyzing a wide range of oribatid mite species living in the same habitat, the study of Schneider et al. (2004) confirmed these observations and thereby received considerable attention. Based on oribatid mites sampled in different forests the study brought realism into previously scattered investigations of the feeding mode of decomposer soil mesofauna. Much previous knowledge derived from laboratory observations of species kept under artificial conditions and offered food materials without choice. For example, mites of the genus Hypochthonius were shown to consume fungi (Maraun et al. 1998) and algae (Norton and Behan-Pelletier 2009), but also living and dead animals, i.e. they can function as predators or necrophages (Riha 1951). High 15N/14N ratios of Hypochthonius rufulus in the study of Schneider et al. (2004) suggest that this species in fact predominantly lives on an animal diet, presumably nematodes or other small and slow moving soil invertebrates which these rather slow moving mites are able to catch, or on their dead remains. Similarly, stable isotope analyses support early assumptions of the diet of the bark-living species Mycobates parmeliae, which was been named after lichens of the genus Parmelia in which it is often
found. Lichens are characterized by very specific stable isotope signatures (low 15N/14N and high 13C/12C ratios), which separate lichens from most other food resources (Fischer et al.
2010); therefore, oribatid mite species with signatures close to the lichens in which they live are likely to also feed on them.
One of the remarkable findings of Schneider et al. (2004) was that a given oribatid mite species appears to occupy a very similar trophic niche even if living in rather different forests.
Earlier findings based on stable isotope ratios suggested that trophic niches of soil invertebrates also differ little with soil depth (Scheu and Falca 2000). Further, Schneider et al.
(2004) found little difference between signatures of adult and juvenile oribatid mite species, suggesting that trophic niches change little during ontogeny. Overall, these results point to a remarkable constancy of trophic niches in oribatid mites and presumably also other soil mesofauna, such as Collembola (Chahartaghi et al. 2005). Constancy and discreteness of trophic niches is particularly surprising considering the wide range of food materials of decomposer soil invertebrates, such as oribatid mites and Collembola, consume if offered in the laboratory (Ruess et al. 2005a). The similarity of a species’ stable isotope signature in different habitats (calibrated to stable isotope ratios of the predominant litter material) and in different studies further indicates that trophic niches vary little over time. Temporal constancy also is surprising as litter materials enter the decomposer system in a pulsed way - particularly in temperate forest ecosystems - and are colonized and broken down by a succession of different fungal species (Hudson 1968, Hayes 1979, Osono 2007). However, detailed data on temporal changes in stable isotope signatures in soil animal species remains scarce, so general conclusions on changes in trophic niches in time and space are difficult to draw. Also, the conclusion that trophic niches of oribatid mite species change little during ontogeny may be premature and needs further investigation. Generally, little is known about differences in feeding habits between juveniles and adults in oribatid mites and other soil invertebrates;
stable isotope analyses may be particularly helpful in elucidating if marked changes in morphology in phylogenetically derived species - such as brachypyline oribatid mites - are associated with shifts in diets.
Recent analyses of stable isotope signatures of bark-living oribatid mites (Erdmann et al.
2007) support the conclusion of Schneider et al. (2004) that individual species occupy distinct trophic niches. However, as with soil species, the exact food materials of bark-living species remains unclear; their stable isotope ratios do not match the signatures of potential food resources analyzed so far, indicating that they feed on cryptic resources, potentially algae or filamentous fungi that decompose bark residues. Surprisingly, we could not ascribe a single
oribatid mite species to moss-feeding despite their collective common name, “moss mites”.
Mosses are characterized by low 13C/12C and 15N/14N ratios (Bokhorst et al. 2007, Fischer et al.
2010), which should allow identification of their consumers.
3. Recent progress
In Figure 1 we summarize recently obtained stable isotope data (15N/14N; 13C/12C) from the bark of trees (Fischer et al. 2010) and from soil (G. Erdmann, unpublished data). Compilation of data from different habitats needs calibration as stable isotope ratios of primary producers may differ. We calibrated the data based on members of the genus Ceratozetes that occurred in both habitats; i.e. Ceratozetes gracilis from soil in the Hainich = Ceratozetes minutissimus from bark in Austria (in the figure only C. gracilis is indicated) since no species simultaneously occurred on the bark of trees and in soil. Using such a calibration the stable isotope data of the soil living oribatid mite species remained unchanged whereas the signatures of the bark living species were slightly changed. The δ15N values of bark itself and of oribatid mites from the bark are much lower than those from litter and soil, which agrees with Schneider et al. (2004) and Heethoff et al. (2009).
The combined analysis of 15N/14N and 13C/12C ratios of oribatid mites indicates that both are useful in delineating the structure of soil and bark food webs and the identification of food resources of oribatid mites. Since 13C is only little enriched in consumers (Wada and Minagawa 1984, Post 2002, Martinez del Rio et al. 2009), it has been dismissed as a useful indicator of the trophic structure of soil communities (Ponsard and Arditi 2000). However, as indicated by our compilation of data (Fig. 1) and others (Schmidt et al. 2004, Tiunov 2007), δ13C values in fact may be a valuable tool to disentangle the trophic structure of soil and bark living invertebrates.
In combination with δ15N values this suggests that the differences in the species composition of arthropods living on bark and in soil correlate with differences in food resources. Further, as documented recently, δ13C values of decomposer animals may allow us to disentangle the components of the litter material that detritivorous animals actually feed on (Pollierer et al.
2009). Also, the combined analysis of δ15N and δ13C values may help us to distinguish organisms feeding on saprotrophic fungi from those feeding on ectomycorrhizal fungi since ectomycorrhizal fungi are enriched in 15N and depleted in 13C, compared to saprophages (Hobbie et al. 2007, 2009).
δ13C values of oribatid mites have also presented surprises. Some oribatid mites, mainly in the Ptyctima but also in a few other taxa, such as the brachypyline genera Carabodes and Liacarus, are enriched in 13C (Fig. 1). It is known that Ptyctima and Carabodes species incorporate calcium carbonate to harden their exoskeleton (Norton and Behan-Pelletier 1991) and this probably is reflected in their 13C signature. Presumably, these species use CO2 from their metabolism and calcium-rich diets to form calcium carbonate minerals in their cuticle (Norton and Behan-Pelletier 1991). A similar process has been described in the earthworm Lumbricus terrestris but here the formed calcium carbonate minerals are excreted as granules, presumably enhancing metabolic CO2 discharge (Canti 2009). If the carbonate is removed from the mites by addition of dilute HCl prior to stable isotope analysis, the 13C signature decreases by about 4 δ units (M.M. Pollierer, unpublished data; see signatures of Steganacarus magnus in Fig. 1). Interestingly, oribatid mite adults with atypical signatures are endophagous as juveniles, burrowing in decaying woody substrates or hard fungal sporophores as e.g., many Carabodes species (Norton and Behan-Pelletier 2009). In future studies using stable isotope signatures of animals that incorporate calcium carbonate in their cuticle those species should always be measured before and after the addition of diluted HCl.
Stable isotope fractionation in below ground food webs from food resources (litter, roots, soil) to consumers (decomposer animals) differs greatly from that of above ground food webs.
Usually, the δ15N values of decomposers are only slightly higher than those of their resource, whereas the δ13C values are much higher (about 3-4 delta units). This enigma may at least in part be solved by the different stable isotope signatures of the respective food components that are included in litter, i.e. lignin, cellulose, starch, lipids, proteins and sugars (Bowling et al.
2008). The δ13C values of those components differ by about six delta units, and consumers only assimilate some components explaining their strong enrichment. In the future it is therefore highly recommended to measure not just the stable isotope signatures of potential food resources of decomposer animals but also those of the respective components (Pollierer et al.
2009).
The naturally high δ13C values of C4 plants, such as maize, sorghum and sugar cane, can be used for tracer experiments. These plants can be grown in the laboratory or in the field and their shoots and/or roots can be exposed in experimental plots of C3 plants; this allows following their characteristic 13C signal in the soil microbial and animal food webs (Oelbermann et al. 2008, Schallhart et al. 2009). Establishing a litter-exchange experiment in the framework of the Swiss Canopy Crane Project (Körner et al. 2005) allowed separation of the role of leaf
litter and root-derived resources for soil animal nutrition, showing that most of the carbon incorporated by soil animals originated from roots rather than leaf litter (Pollierer et al. 2007).
Fig. 1 Mean (± standard deviation) of 13C and 15N values of oribatid mite species and potential food resources (names underlined, in italics, symbols as open circles) in the Hainich forest in Germany and from a small forest stand in Fliess (Austria). Green circles group lichens and lichen feeders, mosses are marked in blue; decomposing material and primary decomposers are marked and circled in black;
oribatid mite taxa that are endophagous as juveniles are marked and circled in brown; secondary decomposer/fungal feeding taxa are marked and circled in grey; and predatory/scavenging species are marked and circled in red; circles are drawn by eye. Using a calibration the stable isotope data of the soil living oribatid mite species remained unchanged, whereas the signatures of the bark living species were slightly changed (for details see text). See Table 1 for full names of oribatid mite species, potential food resources and number of replicates measured. Most data from mosses, lichens and lichen feeding oribatid mites (in green) are from Fischer et al. (2010); other data are from the Hainich, a beech forest in Germany (G. Erdmann, unpublished data).
